Genetic variation in the species Arabidopsis thaliana reveals the existence of natural heat resilience factors for meiosis

Abstract

Heat interferes with multiple meiotic processes leading to genome instability and sterility in flowering plants, including many crops. Despite its importance for food security, the mechanisms underlying heat tolerance of meiosis are poorly understood. In this study, we analyzed different meiotic processes in the Arabidopsis (Arabidopsis thaliana) accessions Columbia (Col) and Landsberg erecta (Ler), their F1 hybrids and F2 offspring under heat stress (37{degrees}C). At 37{degrees}C, Col exhibits significantly reduced formation of double-stand breaks (DSBs) and completely abolished homolog pairing, synapsis and crossover (CO) formation. Strikingly, Ler and Ler/Col hybrids are much less affected than Col. Interestingly, only 10% [~] 20% of F2 offspring exhibit the same heat tolerance of meiotic recombination as parents, indicating that heat resilience in Ler is controlled by the interplay of several loci. Moreover, F2 offspring show defective chromosome condensation in interkinesis, and untimely sister-chromatid segregation and/or chromosome fragmentation, the levels of which exceed those in either inbreds and/or hybrids thus implying a transgressive effect on heat tolerance of meiosis. Furthermore, correlation and cytogenetic analysis suggest that homolog pairing and/or synapsis have an impact on heat tolerance of chromosome morphology and stability during post-recombination stages under heat stress. Taken together, this study reveals the existence of natural heat resilience factors for meiosis in Arabidopsis, which have the great potential to be exploited in breeding programs. Author summaryEnvironmental temperature alterations affect meiotic recombination and/or chromosome segregation thus perturbing genetic makeup and genome stability in plants. We have previously reported that CO formation is fully abolished in Arabidopsis thaliana accession Col under heat stress (36{degrees}C-38{degrees}C) due to reduced DSB formation and impaired homolog pairing. Here, we show that in Arabidopsis thaliana accession Ler under the same high temperature conditions, both DSB and CO formation occur normally, and homolog pairing is mildly impacted, which indicate a striking difference in heat tolerance of meiotic recombination from Col. Remarkably, Col/Ler hybrids display the same heat tolerance as Ler, however, only 10% [~] 20% of F2 offspring behave the same as parents. Moreover, we found higher levels of defects in chromosome morphology and integrity, and sister-chromatid segregation in F2 population than those in both inbreds and hybrids, which suggest a transgressive effect influencing heat tolerance of meiosis. Our findings reveal that heat resilience in Arabidopsis is controlled by the interplay of multiple genomic loci, holding a great potential to be exploited in crop breeding.